Interaction of pheromones during food exploitation by the termite Schedorhinotermes lamanianus

Abstract. Chemical signals from secretions of different exocrine glands modulate a variety of behavioural patterns in termite societies. These signals have multiple functions and may be interactive. During food exploitation workers of the African termite Schedorhinotermes lamanianus (Isoptera: Rhinotermitidae) employ, on foraging trails, the secretion from the sternal gland both for orientation and recruitment to a food source. The secretion from the labial gland, released onto the food by gnawing termites, stimulates additional workers to gnaw at the same site, thereby forming aggregations of gnawing termites. An interaction between these two pheromones during food exploitation is demonstrated for the first time. The volatile signal from the sternal gland inhibits in a dose-dependent manner the non-volatile, highly persistent, signal from the labial gland. The development of gnawing aggregations is inhibited and established ones are dissolved. Behavioural evidence for the perception of both the volatile signal from the sternal gland by olfactory neurones and of the non-volatile signal from the labial gland by gustatory neurones on the antennae is given. The interaction of the two pheromones as a basis for the development of distinct commuting and gnawing zones on the food source, and as a means for a dynamic regulation of food exploitation, is discussed.     

黑胸散白蚁下唇腺的解剖和扫描电镜观察

【目的】通过研究黑胸散白蚁Reticulitermes chinensis下唇腺解剖构造及其在不同品级个体间的分化,为进一步探索口交哺和品级分化机制提供参考。【方法】通过显微解剖观察,了解黑胸散白蚁下唇腺的形态构造及其在不同品级个体间的分化;通过扫描电镜观察,了解下唇腺的结构及神经支配;通过饮水实验,研究工蚁饮水及下唇腺囊的贮水功能。【结果】黑胸散白蚁下唇腺是左右对称结构,每侧构造由一个下唇腺腺泡群、一个下唇腺囊及相关的导管组成。每侧导管分别开口于舌基部下方。蚁后的下唇腺最发达,在下唇腺大小、下唇腺囊大小、腺泡大小及腺泡数量4方面均显著高于其他品级个体;兵蚁、工蚁、有翅成虫的下唇腺也较为发达,相互之间这4个参数的差异性不显著。扫描电镜观察发现,工蚁下唇腺腺泡由主导管和分支导管相连,腺泡外侧有神经分布。黑胸散白蚁工蚁有饮水习性,获得的水贮存在下唇腺囊内。【结论】黑胸散白蚁不同品级个体间,蚁后的下唇腺最发达,有翅成虫的下唇腺也比较发达,说明蚁后除行使生殖职能外,还承担交哺育幼等职能。黑胸散白蚁工蚁有饮水习性,下唇腺囊有贮水功能。     

Reduced cephalic labial glands in the male bumblebees of the subgenus Rhodobombus Dalla Torre (Hymenoptera: Apidae: Bombus Latreille)

Until now, all males of bumblebees are known to attract conspecific females by marking places with a chemical signal secreted by their cephalic labial gland. The specific combination of patrolling flight and scentmarking is of outmost importance to bumblebees as it is their main species specific recognition system. We report here the lack of that recognition system in species of the subgenus Rhodobombus by comparing the morphology and histology of the cephalic labial glands of Bombus (Rhodobombus) mesomelas with those of a well known species, B. (Bombus) terrestris (L.) The cephalic labial glands are much smaller in B. mesomelas than in other bumblebees species and most likely non-functional. This morphology is also observed in B. pomorum and B. brodmanni which also belong to the subgenus Rhodobombus. Our morphological observations are consistent with the chemical analyses of the secretions in B. mesomelas and B. pomorum which are very limited and of most unusual composition for a bumblebee. In addition, whereas other species are thought to use their barbae mandibularis to spread their secretion onto the substrate, these structures are absent in all Rhodobombus. All these observations would mean that the males of Rhodobombus do not attract females from far away by the use of their cephalic labial gland secretions.     

Exocrine glands of the ant Myrmoteras iriodum

This paper describes the morphological characteristics of nine major exocrine glands in workers of the formicine ant Myrmoteras iriodum. The elongate mandibles reveal along their entire length a conspicuous intramandibular gland, which contains both class‐1 and class‐3 secretory cells. The secretory cells of the mandibular glands show a peculiar appearance, with a branched end apparatus, which is unusual for ants. The other major glands (pro‐ and postpharyngeal gland, infrabuccal cavity gland, labial gland, metapleural gland, venom gland and Dufour gland) show common features for formicine ants. The precise function of the glands could not yet be experimentally demonstrated, and to clarify this will depend on the availability of live material of these enigmatic ants in future.     

The labial gland system of larvae of the imported fire ant,Solenopsis invicta Buren

Summary The authors describe the ultrastructure of the labial gland system in imported fire ant larvae, Solenopsis invicta Buren and present an enzyme analysis of enzymes in labial-gland secretions and midgut contents. The tubes of the labial gland produce and secrete a proteinaceous substance rich in digestive enzymes. The narrow cells of the reservoir of the gland have little or no secretory function but the lumen stores the proteinaceous secretion. The labial-gland enzymes include proteases and amylases, which function in extraintestinal digestion of solid food placed on the anteroventral body region of 4th-instar larvae by adult workers. The midgut contains proteases, amylases, and upases. Lipids appear to be predigested by the workers before being fed to the larvae.Approved as TA 15262 by the Director of the Texas Agricultural Experiment Station in cooperation with ARS/USDA. Supported by the Texas Department of Agriculure interagency agreement IAC-0487 (78-79)We would like to thank Rosemary Kamas, Dr. John Mirenda, and Mike Strand for their help in dissections of larvae and Dr. Howard Williams for his advice and suggestions     

Chemical reproductive traits of diploid Bombus terrestris males: Consequences on bumblebee conservation

The current bumblebee decline leads to inbreeding in populations that fosters a loss of allelic diversity and diploid male production. As diploid males are viable and their offspring are sterile, bumblebee populations can quickly fall in a vortex of extinction. In this article, we investigate for the first time a potential premating mechanism through a major chemical reproductive trait (male cephalic labial gland secretions) that could prevent monandrous virgin queens from mating with diploid males. We focus our study on the cephalic labial gland secretions of diploid and haploid males of Bombus terrestris (L.). Contrary to initial expectations, our results do not show any significant differentiation of cephalic labial gland secretions between diploid and haploid specimens. Queens seem therefore to be unable to avoid mating with diploid males based on their compositions of cephalic labial gland secretions. This suggests that the vortex of extinction of diploid males could not be stopped through premating avoidance based on the cephalic labial gland secretions but other mechanisms could avoid mating between diploid males and queens.     

Aquaporin water channel in the salivary glands of the Formosan subterranean termite Coptotermes formosanus is predominant in workers and absent in soldiers

Termite society is unique because the worker caste fetches and carries free water, utilizing it as a solvent for nest construction and gallery building and to maintain wetness for their nestmates. Such water management in a social organization relies largely upon the function of the workers in the colony, as well as on the individuals controlling the location and movement of water inside their bodies. The movement of water via aquaporins (AQPs; water channels) into and out of cells is a key feature of the numerous physiological functions related to whole‐insect water balance. In the present study, the homologue of the water‐specific Drosophila AQP [Drosophila integral protein (DRIP)] is characterized in workers of the Formosan subterranean termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), a highly active wood decomposer. Immunoblot analysis of DRIP‐type AQP using an antibody from the silkworm Bombyx mori reveals that the Coptotermes DRIP (formerly cloned as ‘CfAQP1’) with a molecular mass of approximately 25.7 kDa is expressed predominantly in the salivary (labial) gland of the workers. The Coptotermes DRIP is present at the basal plasma membrane of the parietal cells, as demonstrated by immunocytochemistry. By contrast, there is no DRIP detected within the salivary glands of soldier termites, and neither caste expresses DRIP in their labial gland reservoir (water sac), a tissue that is suggested to have a function as a water sink. The AQP present in the salivary glands is of physiological importance with respect to salivation, aiding in the secretion of cellulolytic enzymes for wood ingestion by the workers of the subterranean termite.     

Comparative Study of the Labial Gland Secretion in Termites (Isoptera)

Labial glands are present in all castes and developmental stages of all termite species. In workers, their secretion contains a food-marking pheromone and digestive enzymes, while soldier secretion plays a defensive role. However, these functions were studied only in a limited set of species, and do not allow drawing general conclusions. Hence, we have investigated the chemical composition of the labial gland extracts from soldiers and workers in 15 termite species belonging to 6 families using an integrative approach based on proteomic and small-molecule profiling. We confirmed the presence of hydroquinone and cellulase in the labial glands of workers, and we identified new toxic compounds in soldiers and workers of several species. Our results highlight the dual role of labial gland secretion, i.e. the defensive role in soldiers and workers of several termite species, and the digestive function in workers.     

Bumble bees alert to food with pheromone from tergal gland

Foragers of Bombus terrestris are able to alert their nestmates to the presence of food sources. It has been supposed that this happens at least partially through the distribution of a pheromone inside the nest. We substantiate this claim using a behavioral test in which an alerting signal is transmitted from one colony to another by long distance air transport, so excluding all other modalities of information exchange. We then investigated the source of the pheromone and were able to show that a hexane extract from tergites V-VII of bumble bee workers elicits higher activity, like a successful forager does. Extracts from other glands, such as the mandibular, labial, hypopharyngeal, and Dufour's gland as well as extracts from other parts of the cuticle had no effect. This suggests that bumble bees possess a pheromone-producing gland, similar to the Nasanov gland in honey bees. Indeed, an extract from the honey bee Nasanov gland also proved to alert bumble bee workers, suggesting a possible homology of the glands.     

Age-dependent changes in ultrastructure of the defensive glands of Neocapritermes taracua workers (Isoptera,Termitidae)

Protection against predators and competitors is one of the main concerns of termite colonies, which developed a specialised defensive caste, the soldiers. However, soldiers are rare or even missing in several lineages of termites, while workers often develop new defence strategies especially in soil-feeding species. Here, we describe the morphology and ultrastructure of the autothysis-associated glands of Neocapritermes taracua workers and report their age-related changes in structure. The defensive glands of N. taracua workers consist of a pair of labial and a pair of crystal glands, whose secretions mix together through autothysis. Autothysis always occurs at the line of weakness connecting the anterior parts of the crystal-bearing pouches. The crystal glands consist of groups of bicellular secretory units (secretory and corresponding canal cells) which secrete the blue crystal material into external pouches. Their secretory activity is maximal in the middle of worker life, and is considerably lower in very young and old workers. The labial glands are composed of two types of secretory cells: the central and the parietal cells. While the central cells are developed similarly to other termites and secrete proteinaceous secretion into labial gland ducts, the parietal cells develop proteinaceous granules which may eventually bud off the cells. The secretory function of parietal cells is so far unique to N. taracua and differs from other termite species in which they are only responsible of water uptake by acini. The defensive device of N. taracua is truly exceptional as it involves a new gland and a previously undescribed function for parietal cells, being a remarkable example of evolution of morphological innovation.     

Morphological and Histochemical Study of Cephalic Glands of Bothrops jararaca (Ophidia,Viperidae)

Morphological and histochemical studies of the cell types in the cephalic glands of Bothrops jararaca have been performed. It is concluded: 1) mucous cells are found in the salivary labial, accessory glands; mucous-serous cells are found in the salivary labial, accessory and Harderian glands; serous-mucous cells are found only in the venom gland; 2) neutral mucosubstances and protein were found in the salivary labial, venom, accessory and Harderian glands; 3) hyaluronic acid was detected in the Harderian gland; 4) of the to sulfated acid mucosubstances, only chondroitin sulfate B was detected in the salivary labial and accessory glands; 5) sialic acid was detected in the salivary labial, accessory and Harderian glands.     

Fine Structure of the Labial Gland in Macrotermes bellicosus (Isoptera,Termitidae)

The labial gland in M. bellicosus corresponds with the acinar type, and occupies the greater part of meso- and metathorax. The acini comprise three secretory cell types, in addition to the central ductule cells and the epithelial cells that make up the efferent ducts. Cell types are mainly distinguished by the size and appearance of their secretory vesicles and the extent of the microvillar contact area with the ductule cells. They probably produce a proteinaceous secretion that may contain digestive enzymes. The labial gland acini in soldiers, on the other hand, contain only one type of secretory cell, which is not comparable with any of the cell types in the worker caste. This difference is in agreement with the multifunctional role of the labial gland according to the termites' polyethism.     

Labial Gland and Its Protein Patterns of Hydropsychid Caddisfly (Hydropsyche kozhantschikovi Martynov: Trichoptera)

ABSTRACT There is a pair of labial gland of hydropsychid caddisfly ( Hydropsyche kozhantschikovi Martynov) larva. It is in 'Z' formation in the body and the total length is about 20 mm. Hydropsychid caddishfly larvae that were raised under the lab conditions were able to form a nest-spining by connecting the small grains of sand provided. By repeatedly treating the extracted labial gland with methanol/D.W., the cell layer was removed. Accordingly, only the matrix within the labial gland that did not dissolve in water was obtained. The matrix inside the methanol/D.W. treated labial gland was dissolved with 5% acetic acid. Then the results of an acidic electrophoresis with a number of conditions indicated that 5% acetic acid/ 5 M urea/ 8% PAGE was the most effective. Moreover, the result of 2-D PAGE on the labial gland of these hydropsychid caddisfly larva, the number of proteins in the labial gland including the cell layer was about 350 and the number of proteins in the labial gland treated with methanol/D.W. was about 80, showing a substantially small number of proteins.     

Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae)

The soldier caste represents the most conspicuous realization of termite eusociality, characterized by an extreme anatomical, behavioural, and physiological specialization. Numerous strategies have evolved in soldiers, including extreme adaptations such as self‐sacrifice by autothysis. In the present study, we investigated the structure and function of defensive glands in Glossotermes oculatus soldiers aiming to understand their use in combat. Three glands are involved in defence: labral, frontal, and labial glands. Mandibles are used to bite the enemy, whereas the secretions of labral and labial glands are discharged into the wound. A striking characteristic of G. oculatus is the lack of the frontal pore; the secretion of the frontal gland is discharged by a rupture of the body wall. We hypothesized that this self‐sacrifice is an efficient way of blocking a gallery under attack. A similar development of the frontal gland occurs in Serritermes serrifer, which supports the close relationship between the two genera inferred from morphological and genetic analyses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 839–848.     

Labial gland disease in the genusFormica (Formicidae,Hymenoptera)

Summary Labial gland disease causes swelling of the labial glands in the pupal stage inFormica species. The resulting adults have enlarged thoraces and are called secretergates (Wasmann's pseudogynes). They infect the younger larvae, probably during feeding. The agent of the disease is unknown. It soon becomes non-infectious outside the labial glands. Diseased females were not seen to feed larvae. Yet their offspring contained secretergates. The discrepancy remains unexplained.     

A stingless bee uses labial gland secretions for scent trail communication (<Emphasis Type="Italic">Trigona recursa</Emphasis> Smith 1863)

The pheromones used by several species of stingless bees for scent trail communication are generally assumed to be produced by the mandibular glands. Here we present strong evidence that in Trigona recursa these pheromones originate from the labial glands, which are well developed in the heads of foragers. Analysis of the behavior involved in scent marking shows that a bee extends her proboscis and rubs it over the substrate. A single scent marking event lasts for 0.59±0.21 s while the bee runs a stretch of 1.04±0.37 cm on a leaf. According to choice experiments the bees are attracted by a feeder baited with labial gland extract (84.2±6% of the bees choose this feeder) but repelled from a feeder baited with mandibular gland extract (only 27.5±13.1% of the bees choose this feeder). They do not discriminate between two clean feeders (49.6±3% of the bees at a feeder). 87±5.1% of bees already feeding leave the feeder after the application of mandibular gland extract whereas only 6.2±4.9% and 2.6±4% do so when labial gland extract or pure solvent was applied.     

The cephalic labial gland secretions of two socially parasitic bumblebees Bombus hyperboreus (Alpinobombus) and Bombus inexspectatus (Thoracobombus) question their inquiline strategy

Social parasitic Hymenopterans have evolved morphological, chemical, and behavioral adaptations to overcome the sophisticated recognition and defense systems of their social host to invade host nests and exploit their worker force. In bumblebees, social parasitism appeared in at least 3 subgenera independently: in the subgenus Psithyrus consisting entirely of parasitic species, in the subgenus Alpinobombus with Bombus hyperboreus, and in the subgenus Thoracobombus with B. inexspectatus. Cuckoo bumblebee males utilize species‐specific cephalic labial gland secretions for mating purposes that can impact their inquiline strategy. We performed cephalic labial gland secretions in B. hyperboreus, B. inexspectatus and their hosts. Males of both parasitic species exhibited high species specific levels of cephalic gland secretions, including different main compounds. Our results showed no chemical mimicry in the cephalic gland secretions between inquilines and their host and we did not identify the repellent compounds already known in other cuckoo bumblebees.     

Novel thoracic glands in the ant Myopias hollandi

Besides the common labial and metapleural glands, four novel exocrine glands are described in the thorax of both workers and queens of the ponerine ant Myopias hollandi. From anterior to posterior, these glands were designated as the propleural pit gland, the posterolateral pronotal gland, the anterolateral propodeal gland and the metasternal process gland. They all correspond with class-3 glands, that are made up of bicellular units that each comprise a secretory cell and a duct cell. In the propleural pit gland, the ducts are characterized by a gradually widening diameter, while in the three other glands the ducts show a portion which displays a balloon-like expansion, that on semithin sections stains very dark. For none of these novel glands the function is known as yet, although ultrastructural examination indicates that they produce a non-proteinaceous and therefore possibly pheromonal secretion.     

Exocrine glands of Lepeophtheirus salmonis (Copepoda: Caligidae): Distribution,developmental appearance,and site of secretion

Exocrine glands of blood‐feeding parasitic copepods are believed to be important in host immune response modulation and inhibition of host blood coagulation, but also in the production of substances for integument lubrication and antifouling. In this study, we aimed to characterize the distribution of different types of salmon louse (Lepeophtheirus salmonis) exocrine glands and their site of secretion. The developmental appearance of each gland type was mapped and genes specifically expressed by glands were identified. Three types of tegumental (teg 1–3) glands and one labial gland type were found. The first glands to appear during development were teg 1 and teg 2 glands. They have ducts extending both dorsally and ventrally suggested to be important in lubricating the integument. Teg 1 glands were found to express two astacin metallopeptidases and a gene with fibronectin II domains, while teg 2 glands express a heme peroxidase. The labial glands were first identified in planktonic copepodids, with reservoirs that allows for storage of glandular products. The last gland type to appear during development was named teg 3 and was not seen before the preadult I stage when the lice become more virulent. Teg 3 glands have ducts ending ventrally at the host‐parasite contact area, and may secrete substances important for the salmon lice virulence. Salmon lice teg 3 and labial glands are thus likely to be especially important in the host‐parasite interaction. Proteins secreted from the salmon louse glands to its salmonid host skin or blood represents a potential interface where the host immune system can meet and elicit effective responses to sea lice antigens. The present study thus represents a fundamental basis for further functional studies and identification of possible vaccine candidates. J. Morphol. 277:1616–1630, 2016. © 2016 Wiley Periodicals, Inc.     

Fine Structure of Cephalic Sense Organs in Meloidogyne incognita Males

Amphids, and the cephalic and labial papillae of Meloidogyne incognita males were examined in detail by electron microscopy. Each amphid basically consists of an amphidial gland, a nerve bundle and an amphidial duct. The gland is a broad microvillous organ with a narrow anterior process, which is closely associated with the amphidial duct. A posterior process of the gland contains secretory organelles and proceeds along the esophagus with the lateral cephalic nerve bundle. The nerve bundle penetrates the broad portion of the gland and, subsequently, individual nerve processes (dendrites) separate from one another, thus forming the sensilla pouch which is enveloped by the gland. Anterior to the pouch, the dendrites converge as they enter and eventually terminate in the amphidial duct. The external opening of the duct is a broad slit which separates the cheek, the outermost part of the lateral lip, from the remainder of the lip region. M. incognita males have six inner labial papillae and four outer cephalic papillae which are each innervated by two and one cilia, respectively. In labial papillae, the cilia appear to terminate at the base of a pore opening, whereas in cephalic papillae each cilium terminates beneath the labial cuticle.